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Skeletal Muscle Regenerative Engineering

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Abstract

Skeletal muscles have the intrinsic ability to regenerate after minor injury, but under certain circumstances such as severe trauma from accidents, chronic diseases, or battlefield injuries the regeneration process is limited. Skeletal muscle regenerative engineering has emerged as a promising approach to address this clinical issue. The regenerative engineering approach involves the convergence of advanced materials science, stem cell science, physical forces, insights from developmental biology, and clinical translation. This article reviews recent studies showing the potential of the convergences of technologies involving biomaterials, stem cells, and bioactive factors in concert with clinical translation, in promoting skeletal muscle regeneration. Several types of biomaterials such as electrospun nanofibers, hydrogels, patterned scaffolds, decellularized tissues, and conductive matrices are being investigated. Detailed discussions are given on how these biomaterials can interact with cells and modulate their behavior through physical, chemical, and mechanical cues. In addition, the application of physical forces such as mechanical and electrical stimulation is reviewed as strategies that can further enhance muscle contractility and functionality. The review also discusses established animal models to evaluate regeneration in two clinically relevant muscle injuries: volumetric muscle loss (VML) and muscle atrophy upon rotator cuff injury. Regenerative engineering approaches using advanced biomaterials, cells, and physical forces, developmental cues along with insights from immunology, genetics, and other aspects of clinical translation hold significant potential to develop promising strategies to support skeletal muscle regeneration.

Lay Summary

Skeletal muscle has robust regeneration properties, but in extreme conditions, the regeneration ability is hindered. It remains a common clinical problem that could lead to long-term disability. The available treatments such as muscle flap transposition present various limitations. To address these limitations, promising strategies based on regenerative engineering are being developed. This review article discusses the different approaches to tissue regeneration using the regenerative engineering paradigm. A specific discussion involves biomaterials and their interactions with cells and bioactive molecules. In addition, the advantages of physical and mechanical stimulation in muscle regeneration are discussed.

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References

  1. Laumonier T, Menetrey J. Muscle injuries and strategies for improving their repair. J Exp Orthop. 2016;3:15. https://doi.org/10.1186/s40634-016-0051-7.

    Google Scholar 

  2. Qazi TH, Mooney DJ, Pumberger M, Geißler S, Duda GN. Biomaterials biomaterials based strategies for skeletal muscle tissue engineering : existing technologies and future trends. Biomaterials. 2015;53:502–21. https://doi.org/10.1016/j.biomaterials.2015.02.110.

    Google Scholar 

  3. Brack AS, Rando TA. Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell. 2012;10:504–14. https://doi.org/10.1016/j.stem.2012.04.001.

    Google Scholar 

  4. Shi X. Muscle stem cells in development, regeneration, and disease. Genes Dev. 2006;20:1692–708. https://doi.org/10.1101/gad.1419406.

    Google Scholar 

  5. Ostrovidov S, Hosseini V, Ahadian S, Fujie T, Parthiban SP, Ramalingam M, et al. Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications. Tissue Eng Part B Rev. 2014;20:403–36. https://doi.org/10.1089/ten.TEB.2013.0534.

    Google Scholar 

  6. Laurencin CT, Khan Y. Regenerative engineering. Sci Transl Med. 2012;4:1–3. https://doi.org/10.1126/scitranslmed.3004467.

    Google Scholar 

  7. C.T. Laurencin, Y. Khan. Regenerative engineering. 1st ed. CRC Press; 2013. https://doi.org/10.1201/b14925.

  8. Lo KWH, Jiang T, Gagnon KA, Nelson C, Laurencin CT. Small-molecule based musculoskeletal regenerative engineering. Trends Biotechnol. 2014;32:74–81. https://doi.org/10.1016/j.tibtech.2013.12.002.

    Google Scholar 

  9. Laurencin CT, Nair LS. Regenerative engineering: approaches to limb regeneration and other grand challenges. Regen Eng Transl Med. 2015;1:1–3. https://doi.org/10.1007/s40883-015-0006-z.

    Google Scholar 

  10. Laurencin CT, Nair LS. The quest toward limb regeneration: a regenerative engineering approach. Regen Biomater. 2016:123–5. https://doi.org/10.1093/rb/rbw002.

  11. Negroni E, Gidaro T, Bigot A, Butler-Browne GS, Mouly V, Trollet C. Invited review: stem cells and muscle diseases: advances in cell therapy strategies. Neuropathol Appl Neurobiol. 2015;41:270–87. https://doi.org/10.1111/nan.12198.

    Google Scholar 

  12. Palmieri B, Tremblay JP, Daniele L. Past, present and future of myoblast transplantation in the treatment of Duchenne muscular dystrophy. Pediatr. Transplant. 2010;14:813–9.

    Google Scholar 

  13. Rinaldi F, Perlingeiro RCR. Stem cells for skeletal muscle regeneration: therapeutic potential and roadblocks. Transl Res. 2014;163:409–17. https://doi.org/10.1016/j.trsl.2013.11.006.

    Google Scholar 

  14. Grounds MD, Radley HG, Lynch GS, Nagaraju K, De Luca A. Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol Dis. 2008;31:1–19.

    Google Scholar 

  15. Partridge TA, Morgan JE, Coulton GR, Hoffman EP, Kunkel LM. Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature. 1989;337:176–9. https://doi.org/10.1038/337176a0.

    Google Scholar 

  16. Péault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther. 2007;15:867–77. https://doi.org/10.1038/mt.sj.6300145.

    Google Scholar 

  17. Skuk D, Roy B, Goulet M, Tremblay JP. Successful myoblast transplantation in primates depends on appropriate cell delivery and induction of regeneration in the host muscle. Exp Neurol. 1999;155:22–30.

    Google Scholar 

  18. Hill E, Boontheekul T, Mooney DJ. Designing scaffolds to enhance transplanted myoblast survival and migration. Tissue Eng. 2006;12:1295–304. https://doi.org/10.1089/ten.2006.12.1295.

    Google Scholar 

  19. Gilbert PM, Havenstrite KL, Magnusson KEG, Sacco A, Leonardi NA, Kraft P, et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science (80-. ). 2010;329:1078–81.

    Google Scholar 

  20. Kinoshita I, Roy R, Dugre FJ, Gravel C, Roy B, Goulet M, et al. Myoblast transplantation in monkeys: control of immune response by FK506. J Neuropathol Exp Neurol. 1996;55:687–97.

    Google Scholar 

  21. Périé S, Trollet C, Mouly V, Vanneaux V, Mamchaoui K, Bouazza B, et al. Autologous myoblast transplantation for oculopharyngeal muscular dystrophy: a phase I/IIa clinical study. Mol Ther. 2014;22:219–25. https://doi.org/10.1038/mt.2013.155.

    Google Scholar 

  22. Lee JY, Qu-Petersen Z, Cao B, Kimura S, Jankowski R, Cummins J, et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol. 2000;150:1085–99. https://doi.org/10.1083/jcb.150.5.1085.

    Google Scholar 

  23. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, et al. Identification of a novel population of muscle stem cells in mice. J Cell Biol. 2002;157:851–64. https://doi.org/10.1083/jcb.200108150.

    Google Scholar 

  24. Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M, et al. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc. 2008;3:1501–9. https://doi.org/10.1038/nprot.2008.142.

    Google Scholar 

  25. Deasy BM, Gharaibeh BM, Pollett JB, Jones MM, Lucas MA, Kanda Y, et al. Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell. 2005;16:3323–33. https://doi.org/10.1091/mbc.E05-02-0169.

    Google Scholar 

  26. Rouger K, Larcher T, Dubreil L, Deschamps JY, Le Guiner C, Jouvion G, et al. Systemic delivery of allogenic muscle stem (MuStem) cells induces long-term muscle repair and clinical efficacy in Duchenne muscular dystrophy dogs. Am J Pathol. 2011. https://doi.org/10.1016/j.ajpath.2011.07.022.

  27. Lardenois A, Jagot S, Lagarrigue M, Guével B, Ledevin M, Larcher T, et al. Quantitative proteome profiling of dystrophic dog skeletal muscle reveals a stabilized muscular architecture and protection against oxidative stress after systemic delivery of MuStem cells. Proteomics. 2016;16:2028–42. https://doi.org/10.1002/pmic.201600002.

    Google Scholar 

  28. Chirieleison SM, Feduska JM, Schugar RC, Askew Y, Deasy BM. Human muscle-derived cell populations isolated by differential adhesion rates: phenotype and contribution to skeletal muscle regeneration in mdx/SCID mice. Tissue Eng. Part A. 2012;18:232–41. https://doi.org/10.1089/ten.tea.2010.0553.

    Google Scholar 

  29. Lorant J, Jaulin N, Leroux I, Schleder C, Zuber C, Charrier M, et al. Immunomodulatory properties of human MuStem cells: assessing their impact on adaptive and innate immunity. ESGCT FSGT. 2015. https://doi.org/10.1089/hum.2015.29008.abstracts.

  30. Torrente Y, Belicchi M, Sampaolesi M, Pisati F, Meregalli M, D’Antona G, et al. Human circulating AC133+ stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest. 2004;114:182–95. https://doi.org/10.1172/JCI200420325.

    Google Scholar 

  31. Shi M, Ishikawa M, Kamei N, Nakasa T, Adachi N, Deie M, et al. Acceleration of skeletal muscle regeneration in a rat skeletal muscle injury model by local injection of human peripheral blood-derived CD133-positive cells. Stem Cells. 2009;27:949–60. https://doi.org/10.1002/stem.4.

    Google Scholar 

  32. Negroni E, Riederer I, Chaouch S, Belicchi M, Razini P, Di Santo J, et al. In vivo myogenic potential of human CD133+ muscle-derived stem cells: a quantitative study. Mol Ther. 2009;17:1771–8. https://doi.org/10.1038/mt.2009.167.

    Google Scholar 

  33. Torrente Y, Belicchi M, Marchesi C, D’Antona G, Cogiamanian F, Pisati F, et al. Autologous transplantation of CD133+ stem cells in Duchenne muscle patients. Cell Transplant. 2007;16:563–77.

    Google Scholar 

  34. Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, et al. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development. 2002;129:2773–83. https://doi.org/10.1098/rstb.2000.0631.

    Google Scholar 

  35. Sampaolesi M. Cell therapy of -sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science (80-. ). 2003;301:487–92. https://doi.org/10.1126/science.1082254.

    Google Scholar 

  36. Sampaolesi M, Blot S, D’Antona G, Granger N, Tonlorenzi R, Innocenzi A, et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature. 2006;444:574–9. https://doi.org/10.1038/nature05282.

    Google Scholar 

  37. Berry SE, Liu J, Chaney EJ, Kaufman SJ. Multipotential mesoangioblast stem cell therapy in the mdx/utrn-/-mouse model for Duchenne muscular dystrophy. Regen Med. 2007;2:275–88.

    Google Scholar 

  38. Díaz-Manera J, Touvier T, Dellavalle A, Tonlorenzi R, Tedesco FS, Messina G, et al. Partial dysferlin reconstitution by adult murine mesoangioblasts is sufficient for full functional recovery in a murine model of dysferlinopathy. Cell Death Dis. 2010;1:e61. https://doi.org/10.1038/cddis.2010.35.

    Google Scholar 

  39. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, et al. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat. Cell Biol. 2007;9:255–67. https://doi.org/10.1038/ncb1542.

    Google Scholar 

  40. Tedesco FS, Hoshiya H, D’Antona G, Gerli MFM, Messina G, Antonini S, et al. Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy. Sci. Transl. Med. 2011;3:96ra78. https://doi.org/10.1126/scitranslmed.3002342.

    Google Scholar 

  41. Cossu G, Previtali SC, Napolitano S, Cicalese MP, Tedesco FS, Nicastro F, et al. Intra-arterial transplantation of HLA-matched donor mesoangioblasts in Duchenne muscular dystrophy. EMBO Mol. Med. 2015;7:1513–28. https://doi.org/10.15252/emmm.201505636.

    Google Scholar 

  42. Dezawa M. Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science (80-. ). 2005;309:314–7. https://doi.org/10.1126/science.1110364.

    Google Scholar 

  43. Wernig G, Janzen V, Schäfer R, Zweyer M, Knauf U, Hoegemeier O, et al. The vast majority of bone-marrow-derived cells integrated into mdx muscle fibers are silent despite long-term engraftment. Proc Natl Acad Sci U S A. 2005;102:11852–7. https://doi.org/10.1073/pnas.0502507102.

    Google Scholar 

  44. Matziolis G, Winkler T, Schaser K, Wiemann M, Krocker D, Tuischer J, et al. Autologous bone marrow-derived cells enhance muscle strength following skeletal muscle crush injury in rats. Tissue Eng. 2006;12:361–7. https://doi.org/10.1089/ten.2006.12.361.

    Google Scholar 

  45. Gang EJ, Darabi R, Bosnakovski D, Xu Z, Kamm KE, Kyba M, et al. Engraftment of mesenchymal stem cells into dystrophin-deficient mice is not accompanied by functional recovery. Exp Cell Res. 2009;315:2624–36. https://doi.org/10.1016/j.yexcr.2009.05.009.

    Google Scholar 

  46. von Roth P, Duda GN, Radojewski P, Preininger B, Strohschein K, Röhner E, et al. Intra-arterial MSC transplantation restores functional capacity after skeletal muscle trauma. Open Orthop. J. 2012;6:352–6. https://doi.org/10.2174/1874325001206010352.

    Google Scholar 

  47. Winkler T, Ph D, Von Roth P, Matziolis G, Mehta M, Eng MS, et al. Dose – response relationship of mesenchymal stem cell transplantation and functional regeneration after severe skeletal muscle injury in rats. Eng Part A. 2008;14:1–6.

    Google Scholar 

  48. De Bari C, Dell’Accio F, Vandenabeele F, Vermeesch JR, Raymackers J-M, Luyten FP. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol. 2003;160:909–18. https://doi.org/10.1083/jcb.200212064.

    Google Scholar 

  49. Meng J. The contribution of human synovial stem cells to skeletal muscle regeneration. Neuromuscul Disord. 2010;20:6–15.

    Google Scholar 

  50. Gang EJ. Skeletal myogenic differentiation of mesenchymal stem cells isolated from human umbilical cord blood. Stem Cells. 2004;22:617–24. https://doi.org/10.1634/stemcells.22-4-617.

    Google Scholar 

  51. Mizuno H, Tobita M, Uysal A. Concise review: adipose-derived stem cells as a novel tool for future regenerative medicine, Stem Cells 2012;30:804–10. https://doi.org/10.1002/stem.1076.

  52. Zuk PA. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell. 2002;13:4279–95. https://doi.org/10.1091/mbc.E02-02-0105.

    Google Scholar 

  53. Zuk P. Adipose-derived stem cells in tissue regeneration: a review. Int Sch Res Not. 2013;2013:e713959. https://doi.org/10.1155/2013/713959.

    Google Scholar 

  54. Rodriguez A-M, Pisani D, Dechesne CA, Turc-Carel C, Kurzenne J-Y, Wdziekonski B, et al. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med. 2005;201:1397–405. https://doi.org/10.1084/jem.20042224.

    Google Scholar 

  55. Goudenege S, Pisani DF, Wdziekonski B, Di Santo JP, Bagnis C, Dani C, et al. Enhancement of myogenic and muscle repair capacities of human adipose–derived stem cells with forced expression of MyoD. Mol Ther. 2009;17:1064–72. https://doi.org/10.1038/mt.2009.67.

    Google Scholar 

  56. Di Rocco G, Iachininoto MG, Tritarelli A, Straino S, Zacheo A, Germani A, et al. Myogenic potential of adipose-tissue-derived cells. J Cell Sci. 2006;119:2945–52. https://doi.org/10.1242/jcs.03029.

    Google Scholar 

  57. Vieira NM, Bueno CR, Brandalise V, Moraes LV, Zucconi E, Secco M, et al. SJL dystrophic mice express a significant amount of human muscle proteins following systemic delivery of human adipose-derived stromal cells without immunosuppression. Stem Cells. 2008;26:2391–8. https://doi.org/10.1634/stemcells.2008-0043.

    Google Scholar 

  58. Alexeev V, Arita M, Donahue A, Bonaldo P, Chu M-L, Igoucheva O. Human adipose-derived stem cell transplantation as a potential therapy for collagen VI-related congenital muscular dystrophy. Stem Cell Res Ther. 2014;5:21. https://doi.org/10.1186/scrt411.

    Google Scholar 

  59. Vieira NM, Valadares M, Zucconi E, Secco M, Bueno Junior CR, Brandalise V, et al. Human adipose-derived mesenchymal stromal cells injected systemically into GRMD dogs without immunosuppression are able to reach the host muscle and express human dystrophin. Cell Transplant. 2012;21:1407–17. https://doi.org/10.3727/096368911X.

    Google Scholar 

  60. Shabbir A, Zisa D, Leiker M, Johnston C, Lin H, Lee T. Muscular dystrophy therapy by nonautologous mesenchymal stem cells: muscle regeneration without immunosuppression and inflammation. Transplantation. 2009;87:1275–82. https://doi.org/10.1097/TP.0b013e3181a1719b.

    Google Scholar 

  61. Caplan A, Dennis J. Mesenchymal stem cells as trophic mediators. J Cell Biochem. 2006.

  62. Barberi T, Bradbury M, Dincer Z, Panagiotakos G, Socci ND, Studer L. Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med. 2007;13:642–8. https://doi.org/10.1038/nm1533.

    Google Scholar 

  63. Darabi R, Gehlbach K, Bachoo RM, Kamath S, Osawa M, Kamm KE, et al. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med. 2008;14:134–43. https://doi.org/10.1038/nm1705.

    Google Scholar 

  64. Sakurai H, Okawa Y, Inami Y, Nishio N, Isobe K. Paraxial mesodermal progenitors derived from mouse embryonic stem cells contribute to muscle regeneration via differentiation into muscle satellite cells. Stem Cells. 2008;26:1865–73. https://doi.org/10.1634/stemcells.2008-0173.

    Google Scholar 

  65. Chang H, Yoshimoto M, Umeda K, Iwasa T, Mizuno Y, Fukada S-I, et al. Generation of transplantable, functional satellite-like cells from mouse embryonic stem cells. FASEB J. 2009;23:1907–19. https://doi.org/10.1096/fj.08-123661.

    Google Scholar 

  66. Filareto A, Darabi R, Perlingeiro RCR. Engraftment of ES-derived myogenic progenitors in a severe mouse model of muscular dystrophy. J Stem Cell Res Ther. 2012;10:1–5. https://doi.org/10.4172/2157-7633.S10-001.

    Google Scholar 

  67. Darabi R, Santos F, Filareto A, Pan W, Koene R. Assessment of the myogenic stem cell compartment following transplantation of Pax3/Pax7-induced embryonic stem cell-derived progenitors, Stem Cells. 2011;29:777–90. https://doi.org/10.1002/stem.625.

  68. Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M, Kyba M, et al. Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell. 2012;10:610–9. https://doi.org/10.1016/j.stem.2012.02.015.

    Google Scholar 

  69. Quattrocelli M, Palazzolo G, Floris G, Schöffski P, Anastasia L, Orlacchio A, et al. Intrinsic cell memory reinforces myogenic commitment of pericyte-derived iPSCs. J Pathol. 2011;223:593–603. https://doi.org/10.1002/path.2845.

    Google Scholar 

  70. Tedesco FS, Gerli MFM, Perani L, Benedetti S, Ungaro F, Cassano M, et al. Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci. Transl. Med. 2012;4:140ra89. https://doi.org/10.1126/scitranslmed.3003541.

    Google Scholar 

  71. Yoshida T, Galvez S, Tiwari S, Rezk BM, Semprun-Prieto L, Higashi Y, et al. Angiotensin II inhibits satellite cell proliferation and prevents skeletal muscle regeneration. J Biol Chem. 2013;288:23823–32. https://doi.org/10.1074/jbc.M112.449074.

    Google Scholar 

  72. Majewski RL, Zhang W, Ma X, Cui Z, Ren W, Markel DC. Bioencapsulation technologies in tissue engineering. J Appl Biomater Funct Mater. 2016;14:e395–403. https://doi.org/10.5301/jabfm.5000299.

    Google Scholar 

  73. Lee K, Silva EA, Mooney DJ. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J R Soc Interface. 2011;8:153–70. https://doi.org/10.1098/rsif.2010.0223.

    Google Scholar 

  74. Tallawi M, Rosellini E, Barbani N, Cascone MG, Rai R, Saint-Pierre G, et al. Strategies for the chemical and biological functionalization of scaffolds for cardiac tissue engineering: a review. J R Soc Interface. 2015;12:20150254. https://doi.org/10.1098/rsif.2015.0254.

    Google Scholar 

  75. Passipieri JA, Christ GJ. The potential of combination therapeutics for more complete repair of volumetric muscle loss injuries: the role of exogenous growth factors and/or progenitor cells in implantable skeletal muscle tissue engineering technologies. Cells Tissues Organs. 2016;202:202–13. https://doi.org/10.1159/000447323.

    Google Scholar 

  76. Syverud BC, VanDusen KW, Larkin LM. Growth factors for skeletal muscle tissue engineering. Cells Tissues Organs. 2016;202:169–79. https://doi.org/10.1159/000444671.

    Google Scholar 

  77. Longo UG, Loppini M, Berton A, Spiezia F, Maffulli N, Denaro V. Tissue engineered strategies for skeletal muscle injury. Stem Cells Int. 2012;2012. https://doi.org/10.1155/2012/175038.

  78. Delaney K, Kasprzycka P, Ciemerych MA, Zimowska M. The role of TGF-β1 during skeletal muscle regeneration. Cell Biol. Int. 2017. https://doi.org/10.1002/cbin.10725.

  79. Weist MR, Wellington MS, Bermudez JE, Kostrominova TY, Mendias CL, Arruda EM, et al. TGF-β1 enhances contractility in engineered skeletal muscle. J Tissue Eng Regen Med. 2013;7:562–71. https://doi.org/10.1002/term.551.

    Google Scholar 

  80. Sheehan SM, Allen RE. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J Cell Physiol. 1999;181:499–506. https://doi.org/10.1002/(sici)1097-4652(199912)181:3<499::aid-jcp14>3.0.co;2-1.

    Google Scholar 

  81. Pawlikowski B, Vogler TO, Gadek K, Olwin BB. Regulation of skeletal muscle stem cells by fibroblast growth factors. Dev Dyn. 2017. https://doi.org/10.1002/dvdy.24495.

  82. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev Biol. 1998;194:114–28. https://doi.org/10.1006/dbio.1997.8803.

    Google Scholar 

  83. Arsic N, Zacchigna S, Zentilin L, Ramirez-Correa G, Pattarini L, Salvi A, et al. Vascular endothelial growth factor stimulates skeletal muscle regeneration in vivo. Mol Ther. 2004;10:844–54. https://doi.org/10.1016/j.ymthe.2004.08.007.

    Google Scholar 

  84. Wagner PD. The critical role of VEGF in skeletal muscle angiogenesis and blood flow. Biochem Soc Trans. 2011;39:1556–9. https://doi.org/10.1042/bst20110646.

    Google Scholar 

  85. Witt R, Weigand A, Boos AM, Cai A, Dippold D, Boccaccini AR, et al. Mesenchymal stem cells and myoblast differentiation under HGF and IGF-1 stimulation for 3D skeletal muscle tissue engineering. BMC Cell Biol. 2017;18:15. https://doi.org/10.1186/s12860-017-0131-2.

    Google Scholar 

  86. Hammers DW, Sarathy A, Pham CB, Drinnan CT, Farrar RP, Suggs LJ. Controlled release of IGF-I from a biodegradable matrix improves functional recovery of skeletal muscle from ischemia/reperfusion. Biotechnol Bioeng. 2012;109:1051–9. https://doi.org/10.1002/bit.24382.

    Google Scholar 

  87. Borselli C, Storrie H, Benesch-lee F, Shvartsman D, Cezar C, Lichtman JW. Functional muscle regeneration with combined delivery of angiogenesis and myogenesis factors. 2010;107. doi:https://doi.org/10.1073/pnas.0903875106.

  88. James R, Laurencin C. Musculoskeletal regenerative engineering: biomaterials, structures, and small molecules. Adv Biomater. 2014;201:1–12.

    Google Scholar 

  89. Aravamudhan A, Ramos DM, Nip J, Subramanian A, James R, Harmon MD, et al. Osteoinductive small molecules: growth factor alternatives for bone tissue engineering. Curr. Pharm. Des. 2013;19:3420–8.

    Google Scholar 

  90. Carbone EJ, Rajpura K, Jiang T, Laurencin CT, Lo KW-H. Regulation of bone regeneration with approved small molecule compounds. Adv Regen Biol 2014;1:25276. https://doi.org/10.3402/arb.v1.25276.

  91. Bernacchioni C, Cencetti F, Blescia S, Donati C, Bruni P. Sphingosine kinase/sphingosine 1-phosphate axis: a new player for insulin-like growth factor-1-induced myoblast differentiation. In: Skelet Muscle, 2012: p. 15. doi:https://doi.org/10.1186/2044-5040-2-15.

  92. Maceyka M, Harikumar KB, Milstien S, Spiegel S. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol. 2012;22:50–60. https://doi.org/10.1016/j.tcb.2011.09.003.

    Google Scholar 

  93. Danieli-Betto D, Peron S, Germinario E, Zanin M, Sorci G, Franzoso S, et al. Sphingosine 1-phosphate signaling is involved in skeletal muscle regeneration. Am J Physiol Cell Physiol. 2010;298:C550–8. https://doi.org/10.1152/ajpcell.00072.2009.

    Google Scholar 

  94. Smith CK II, Janney MJ, Allen RE. Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J Cell Physiol. 1994;159:379–85. https://doi.org/10.1002/jcp.1041590222.

    Google Scholar 

  95. Kennedy KAM, Porter T, Mehta V, Ryan SD, Price F, Peshdary V, et al. Retinoic acid enhances skeletal muscle progenitor formation and bypasses inhibition by bone morphogenetic protein 4 but not dominant negative β-catenin. BMC Biol. 2009;7:67. https://doi.org/10.1186/1741-7007-7-67.

    Google Scholar 

  96. Blomhoff R, Blomhoff HK. Overview of retinoid metabolism and function. J Neurobiol. 2006;66:606–30. https://doi.org/10.1002/neu.20242.

    Google Scholar 

  97. Lee H, Haller C, Manneville C, Doll T, Fruh I, Keller CG, et al. Identification of small molecules which induce skeletal muscle differentiation in embryonic stem cells via activation of the Wnt and inhibition of Smad2/3 and sonic hedgehog pathways. Stem Cells. 2016;34:299–310. https://doi.org/10.1002/stem.2228.

    Google Scholar 

  98. Lo KWH, Ashe KM, Kan HM, Laurencin CT. The role of small molecules in musculoskeletal regeneration. Regen Med. 2012;7:535–49.

    Google Scholar 

  99. Wu F, Jin T. Polymer-based sustained-release dosage forms for protein drugs, challenges, and recent advances. In: AAPS PharmSciTech, 2008: pp. 1218–1229. doi:https://doi.org/10.1208/s12249-008-9148-3.

  100. Rowley JA, Mooney DJ. Alginate type and RGD density control myoblast phenotype. J Biomed Mater Res. 2002;60:217–23. https://doi.org/10.1002/jbm.1287.

    Google Scholar 

  101. Fu C, Ziegler F. Vibration prone multi-purpose buildings and towers effectively damped by tuned liquid column-gas dampers. Asian J Civ Eng. 2009;10:21–56. https://doi.org/10.2217/nnm.10.12.Engineering.

    Google Scholar 

  102. Li WJ, Laurencin CT, Caterson EJ, Tuan RS, Ko FK. Electrospun nanofibrous structure: a novel scaffold for tissue engineering. J Biomed Mater Res. 2002;60:613–21. https://doi.org/10.1002/jbm.10167.

    Google Scholar 

  103. Nair LS, Bhattacharyya S, Laurencin CT. Development of novel tissue engineering scaffolds via electrospinning. Expert Opin Biol Ther. 2004;4:659–68. https://doi.org/10.1517/14712598.4.5.659.

    Google Scholar 

  104. Laurencin CT, Kumbar SG, Nukavarapu SP, James R, Hogan MV. Recent patents on electrospun biomedical nanostructures: an overview. Recent Pat Biomed Eng. 2008;1:68–78. https://doi.org/10.2174/1874764710801010068.

    Google Scholar 

  105. Jiang T, Carbone EJ, Lo KW-H, Laurencin CT. Electrospinning of polymer nanofibers for tissue regeneration. Prog Polym Sci. 2015;46:1–24. https://doi.org/10.1016/j.progpolymsci.2014.12.001.

    Google Scholar 

  106. Nair LS, Bhattacharyya S, Bender JD, Greish YE, Brown PW, Allcock HR, et al. Fabrication and optimization of methylphenoxy substituted polyphosphazene nanofibers for biomedical applications. Biomacromolecules. 2004;5:2212–20. https://doi.org/10.1021/bm049759j.

    Google Scholar 

  107. Kumbar SG, Nukavarapu SP, James R, Nair LS, Laurencin CT. Electrospun poly(lactic acid-co-glycolic acid) scaffolds for skin tissue engineering. Biomaterials. 2008;29:4100–7. https://doi.org/10.1016/j.biomaterials.2008.06.028.

    Google Scholar 

  108. Katti DS, Robinson KW, Ko FK, Laurencin CT. Bioresorbable nanofiber-based systems for wound healing and drug delivery: optimization of fabrication parameters. J Biomed Mater Res Part B Appl Biomater. 2004;70:286–96. https://doi.org/10.1002/jbm.b.30041.

    Google Scholar 

  109. Merrell JG, McLaughlin SW, Tie L, Laurencin CT, Chen AF, Nair LS. Curcumin-loaded poly(epsilon-caprolactone) nanofibres: diabetic wound dressing with anti-oxidant and anti-inflammatory properties. Clin Exp Pharmacol Physiol. 2009;36:1149–56. https://doi.org/10.1111/j.1440-1681.2009.05216.x.

    Google Scholar 

  110. Bhattcharyya S, Nair LS, Singh A, Krogman NR, Greish YE, Brown PW, et al. Electrospinning of poly[bis(ethyl alanato) phosphazene] nanofibers. J Biomed Nanotechno. 2006;2:36–45. https://doi.org/10.1166/jbn.2006.008.

    Google Scholar 

  111. Deng M, Kumbar SG, Nair LS, Weikel AL, Allcock HR, Laurencin CT. Biomimetic structures: biological implications of dipeptide-substituted Polyphosphazene–polyester blend nanofiber matrices for load-bearing bone regeneration. Adv Funct Mater. 2011;21:2641–51. https://doi.org/10.1002/adfm.201100275.

    Google Scholar 

  112. Choi JS, Lee SJ, Christ GJ, Atala A, Yoo JJ. The influence of electrospun aligned poly(??-caprolactone)/collagen nanofiber meshes on the formation of self-aligned skeletal muscle myotubes. Biomaterials. 2008;29:2899–906. https://doi.org/10.1016/j.biomaterials.2008.03.031.

    Google Scholar 

  113. Aviss KJ, Gough JE, Downes S. Aligned electrospun polymer fibres for skeletal muscle regeneration. Eur Cells Mater. 2010;19:193–204.

    Google Scholar 

  114. Chen M-C, Sun Y-C, Chen Y-H. Electrically conductive nanofibers with highly oriented structures and their potential application in skeletal muscle tissue engineering. Acta Biomater. 2013;9:5562–72. https://doi.org/10.1016/j.actbio.2012.10.024.

    Google Scholar 

  115. Jun I, Jeong S, Shin H. The stimulation of myoblast differentiation by electrically conductive sub-micron fibers. Biomaterials. 2009;30:2038–47. https://doi.org/10.1016/j.biomaterials.2008.12.063.

    Google Scholar 

  116. Bian W, Bursac N. Tissue engineering of functional skeletal muscle: challenges and recent advances. IEEE Eng Med Biol Mag. 2008;27:109–13. https://doi.org/10.1109/MEMB.2008.928460.

    Google Scholar 

  117. Chikar JA, Hendricks JL, Richardson-Burns SM, Raphael Y, Pfingst BE, Martin DC. The use of a dual PEDOT and RGD-functionalized alginate hydrogel coating to provide sustained drug delivery and improved cochlear implant function. Biomaterials. 2012;33:1982–90. https://doi.org/10.1016/j.biomaterials.2011.11.052.

    Google Scholar 

  118. Juhas M, Bursac N. Engineering skeletal muscle repair. Curr Opin Biotechnol. 2013;24:880–6. https://doi.org/10.1016/j.copbio.2013.04.013.

    Google Scholar 

  119. Borselli C, Cezar CA, Shvartsman D, Vandenburgh HH, Mooney DJ. The role of multifunctional delivery scaffold in the ability of cultured myoblasts to promote muscle regeneration. Biomaterials. 2011;32:8905–14. https://doi.org/10.1016/j.biomaterials.2011.08.019.

    Google Scholar 

  120. Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials. 2010;31:5536–44. https://doi.org/10.1016/j.biomaterials.2010.03.064.

    Google Scholar 

  121. Hinds S, Bian W, Dennis RG, Bursac N. The role of extracellular matrix composition in structure and function of bioengineered skeletal muscle. Biomaterials. 2011;32:3575–83. https://doi.org/10.1016/j.biomaterials.2011.01.062.

    Google Scholar 

  122. Bian W, Bursac N. Engineered skeletal muscle tissue networks with controllable architecture. Biomaterials. 2009;30:1401–12. https://doi.org/10.1016/j.biomaterials.2008.11.015.

    Google Scholar 

  123. CURTIS AS. The mechanism of adhesion of cells to glass. A study by interference reflection microscopy. J. Cell Biol. 1964;20:199–215. https://doi.org/10.1083/jcb.20.2.199.

    Google Scholar 

  124. Yang HS, Ieronimakis N, Tsui JH, Kim HN, Suh KY, Reyes M, et al. Nanopatterned muscle cell patches for enhanced myogenesis and dystrophin expression in a mouse model of muscular dystrophy. Biomaterials. 2014;35:1478–86. https://doi.org/10.1016/j.biomaterials.2013.10.067.

    Google Scholar 

  125. Yang HS, Lee B, Tsui JH, Macadangdang J, Jang S-YY, Im SG, Kim D-HH. Electroconductive nanopatterned substrates for enhanced myogenic differentiation and maturation, Adv. Healthc. Mater. 2015;5. doi:https://doi.org/10.1002/adhm.201500003.

  126. Li K-C, Hwang S-M, Chien H-H, Yuan C-C, Lu H-E, Ma K-J, et al. Submicron-grooved culture surface extends myotube length by forming parallel and elongated motif. Micro Nano Lett. 2013;8:440–4. https://doi.org/10.1049/mnl.2013.0153.

    Google Scholar 

  127. Patz TM, Doraiswamy A, Narayan RJ, Modi R, Chrisey DB. Two-dimensional differential adherence and alignment of C2C12 myoblasts. Mater Sci Eng B Solid-State Mater Adv Technol. 2005;123:242–7. https://doi.org/10.1016/j.mseb.2005.08.088.

    Google Scholar 

  128. Hosseini V, Ahadian S, Ostrovidov S, Camci-Unal G, Chen S, Kaji H, et al. Engineered contractile skeletal muscle tissue on a microgrooved methacrylated gelatin substrate. Tissue Eng. Part A. 2012;18:2453–65. https://doi.org/10.1089/ten.TEA.2012.0181.

    Google Scholar 

  129. El-Mohri H, Wu Y, Mohanty S, Ghosh G. Impact of matrix stiffness on fibroblast function. Mater Sci Eng C. 2017;74:146–51. https://doi.org/10.1016/j.msec.2017.02.001.

    Google Scholar 

  130. Chen S, Nakamoto T, Kawazoe N, Chen G. Engineering multi-layered skeletal muscle tissue by using 3D microgrooved collagen scaffolds. Biomaterials. 2015;73:23–31. https://doi.org/10.1016/j.biomaterials.2015.09.010.

    Google Scholar 

  131. Patel A, Mukundan S, Wang W, Karumuri A, Sant V, Mukhopadhyay SM, et al. Carbon-based hierarchical scaffolds for myoblast differentiation: synergy between nano-functionalization and alignment. Acta Biomater. 2016;32:77–88. https://doi.org/10.1016/j.actbio.2016.01.004.

    Google Scholar 

  132. Valentin JE, Turner NJ, Gilbert TW, Badylak SF. Functional skeletal muscle formation with a biologic scaffold. Biomaterials. 2010;31:7475–84. https://doi.org/10.1016/j.biomaterials.2010.06.039.

    Google Scholar 

  133. Song JJ, Ott HC. Organ engineering based on decellularized matrix scaffolds. Trends Mol Med. 2011;17:424–32. https://doi.org/10.1016/j.molmed.2011.03.005.

    Google Scholar 

  134. Yu X, Tang X, Gohil SV, Laurencin CT. Biomaterials for bone regenerative engineering. Adv Healthc Mater. 2015;4:1268–85. https://doi.org/10.1002/adhm.201400760.

    Google Scholar 

  135. Wolf MT, Daly KA, Reing JE, Badylak SF. Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials. 2012;33:2916–25. https://doi.org/10.1016/j.biomaterials.2011.12.055.

    Google Scholar 

  136. Ward CL, Ji L, Corona BT. An autologous muscle tissue expansion approach for the treatment of volumetric muscle loss. Biores. Open Access. 2015;4:198–208. https://doi.org/10.1089/biores.2015.0009.

    Google Scholar 

  137. Machingal MA, Corona BT, Walters TJ, Kesireddy V, Koval CN, Dannahower A, et al. A tissue-engineered muscle repair construct for functional restoration of an irrecoverable muscle injury in a murine model. Tissue Eng Part A. 2011;17:2291–303. https://doi.org/10.1089/ten.tea.2010.0682.

    Google Scholar 

  138. Corona BT, Ward CL, Baker HB, Walters TJ, Christ GJ. Implantation of in vitro tissue engineered muscle repair constructs and bladder acellular matrices partially restore in vivo skeletal muscle function in a rat model of volumetric muscle loss injury. Tissue Eng. Part A. 2013;20:131219054609007. https://doi.org/10.1089/ten.tea.2012.0761.

    Google Scholar 

  139. Balint R, Cassidy NJ, Cartmell SH. Conductive polymers: towards a smart biomaterial for tissue engineering. Acta Biomater. 2014;10:2341–53. https://doi.org/10.1016/j.actbio.2014.02.015.

    Google Scholar 

  140. Rivers TJ, Hudson TW, Schmidt CE. Synthesis of a novel, biodegradable electrically conducting polymer for biomedical applications. Adv Funct Mater. 2002;12:33. https://doi.org/10.1002/1616-3028(20020101)12:1<33::AID-ADFM33>3.0.CO;2-E.

    Google Scholar 

  141. Guo B, Glavas L, Albertsson A-C. Biodegradable and electrically conducting polymers for biomedical applications. Prog Polym Sci. 2013;38:1263–86. https://doi.org/10.1016/j.progpolymsci.2013.06.003.

    Google Scholar 

  142. Mao C, Zhu A, Wu Q, Chen X, Kim J, Shen J. New biocompatible polypyrrole-based films with good blood compatibility and high electrical conductivity. Colloids Surf B Biointerfaces. 2008;67:41–5. https://doi.org/10.1016/j.colsurfb.2008.07.012.

    Google Scholar 

  143. Lee JY, Bashur CA, Goldstein AS, Schmidt CE. Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials. 2009;30:4325–35. https://doi.org/10.1016/j.biomaterials.2009.04.042.

    Google Scholar 

  144. Sajesh KM, Jayakumar R, Nair SV, Chennazhi KP. Biocompatible conducting chitosan/polypyrrole-alginate composite scaffold for bone tissue engineering. Int. J. Biol. Macromol. 2013;62:465–\\. https://doi.org/10.1016/j.ijbiomac.2013.09.028.

    Google Scholar 

  145. Qazi TH, Rai R, Boccaccini AR. Biomaterials tissue engineering of electrically responsive tissues using polyaniline based polymers : a review. Biomaterials. 2014:1–19. https://doi.org/10.1016/j.biomaterials.2014.07.020.

  146. Peramo A, Urbanchek MG, Spanninga SA, Povlich LK, Cederna P, Martin DC. In situ polymerization of a conductive polymer in acellular muscle tissue constructs. Tissue Eng. Part A. 2008;14:423–32. https://doi.org/10.1089/tea.2007.0123.

    Google Scholar 

  147. Hadjizadeh A, Doillon CJ. Directional migration of endothelial cells towards angiogenesis using polymer fibres in a 3D co-culture system. J Tissue Eng Regen Med. 2010;4:524–31. https://doi.org/10.1002/term.

    Google Scholar 

  148. Gilmore KJ, Kita M, Han Y, Gelmi A, Higgins MJ, Moulton SE, et al. Biomaterials skeletal muscle cell proliferation and differentiation on polypyrrole substrates doped with extracellular matrix components. Biomaterials. 2009;30:5292–304. https://doi.org/10.1016/j.biomaterials.2009.06.059.

    Google Scholar 

  149. Ostrovidov S, Shi X, Zhang L, Liang X, Kim SB, Fujie T, et al. Myotube formation on gelatin nanofibers - multi-walled carbon nanotubes hybrid scaffolds. Biomaterials. 2014;35:6268–77. https://doi.org/10.1016/j.biomaterials.2014.04.021.

    Google Scholar 

  150. Hyoungshin Park RL, Bhalla R, Saigal R, Radisic M, Watson N, Vunjak-Novakovic G. Effects of electrical stimulation in C2C12muscle constructs. J Tissue Eng Regen Med. 2008;2:279–87. https://doi.org/10.1002/term.93.

    Google Scholar 

  151. Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23:47–55. https://doi.org/10.1038/nbt1055.

    Google Scholar 

  152. Cezar CA, Roche ET, Vandenburgh HH, Duda GN, Walsh CJ, Mooney DJ. Biologic-free mechanically induced muscle regeneration. Proc Natl Acad Sci U S A. 2016;113:1534–9. https://doi.org/10.1073/pnas.1517517113.

    Google Scholar 

  153. du Moon G, Christ G, Stitzel JD, Atala A, Yoo JJ. Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng Part A. 2008;14:473–82. https://doi.org/10.1089/tea.2007.0104.

    Google Scholar 

  154. Vandenburgh HH, Karlisch P. Longitudinal growth of skeletal myotubes in vitro in a new horizontal mechanical cell stimulator. In Vitro Cell Dev Biol. 1989;25:607–16.

    Google Scholar 

  155. Abat F, Valles SL, Gelber PE, Polidori F, Stitik TP, García-Herreros S, et al. Molecular repair mechanisms using the intratissue percutaneous electrolysis technique in patellar tendonitis. Rev. Española Cirugía Ortopédica Y Traumatol. (English Ed.). 2014;58:201–5. https://doi.org/10.1016/j.recote.2014.05.005.

    Google Scholar 

  156. Marloes KYR-C, Langelaan LP, Kristel JM, Boonen MJP, Daisy FPTB, van der Schaft WJ. Advanced maturation by electrical stimulation: differences in response between C2C12 and primary muscle progenitor cells. J. Tissue Eng. Regen. Med. 2010;4:524–31. https://doi.org/10.1002/term.

    Google Scholar 

  157. Pette D, Vrbova G. What does chronic electrical stimulation teach us about muscle plasticity? Muscle Nerve. 1999;22:666–77.

    Google Scholar 

  158. Xia Y, Buja LM, Scarpulla RC, McMillin JB. Electrical stimulation of neonatal cardiomyocytes results in the sequential activation of nuclear genes governing mitochondrial proliferation and differentiation. Proc Natl Acad Sci U S A. 1997;94:11399–404. https://doi.org/10.1073/pnas.94.21.11399.

    Google Scholar 

  159. Fujita H, Nedachi T, Kanzaki M. Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp Cell Res. 2007;313:1853–65. https://doi.org/10.1016/j.yexcr.2007.03.002.

    Google Scholar 

  160. Nedachi T, Fujita H, Kanzaki M. Contractile C2C12 myotube model for studying exercise-inducible responses in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2008;295:E1191–204. https://doi.org/10.1152/ajpendo.90280.2008.

    Google Scholar 

  161. Kanno S, Oda N, Abe M, Saito S, Hori K, Handa Y, et al. Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation. 1999;99:2682–7. https://doi.org/10.1161/01.CIR.99.20.2682.

    Google Scholar 

  162. Brutsaert TD, Gavin TP, Fu Z, Breen EC, Tang K, Mathieu-Costello O, et al. Regional differences in expression of VEGF mRNA in rat gastrocnemius following 1 hr exercise or electrical stimulation. BMC Physiol. 2002;2:8. https://doi.org/10.1186/1472-6793-2-8.

    Google Scholar 

  163. van der Schaft DWJ, van Spreeuwel ACC, Boonen KJM, Langelaan MLP, Bouten CVC, Baaijens FPT. Engineering skeletal muscle tissues from murine myoblast progenitor cells and application of electrical stimulation., J. Vis. Exp. 2013; e4267. doi:https://doi.org/10.3791/4267.

  164. Pedrotty DM, Koh J, Davis BH, Taylor DA, Wolf P, Niklason LE. Engineering skeletal myoblasts: roles of three-dimensional culture and electrical stimulation. Am J Physiol Hear Circ Physiol. 2005;288:H1620–6. https://doi.org/10.1152/ajpheart.00610.2003.

    Google Scholar 

  165. N. Burch, A.S. Arnold, F. Item, S. Summermatter, G.B.S. Santos, M. Christe, U. Boutellier, M. Toigo, C. Handschin, Electric pulse stimulation of cultured murine muscle cells reproduces gene expression changes of trained mouse muscle, PLoS One. 2010;5. doi:https://doi.org/10.1371/journal.pone.0010970.

  166. Trumble DR, Changping D, Magovern JA. Effects of long-term stimulation on skeletal muscle phenotype expression and collagen/fibrillin distribution. Basic Appl Myol. 2001;11(2):91–8.

    Google Scholar 

  167. Hamada T, Sasaki H, Hayashi T, Moritani T, Nakao K. Enhancement of whole body glucose uptake during and after human skeletal muscle low-frequency electrical stimulation. J Appl Physiol. 2003;94:2107–12. https://doi.org/10.1152/japplphysiol.00486.2002.

    Google Scholar 

  168. Wolf MT, Dearth CL, Sonnenberg SB, Loboa EG, Badylak SF. Naturally derived and synthetic scaffolds for skeletal muscle reconstruction. Adv Drug Deliv Rev. 2015;84:208–21. https://doi.org/10.1016/j.addr.2014.08.011.

    Google Scholar 

  169. Corona BT, Rivera JC, Owens JG, Wenke JC, Rathbone CR. Volumetric muscle loss leads to permanent disability following extremity trauma. J Rehabil Res Dev. 2015;52:785–92. https://doi.org/10.1682/JRRD.2014.07.0165.

    Google Scholar 

  170. Grogan BF, Hsu MAJJR. Volumetric muscle loss. 2011;19.

  171. Sicari BM, Rubin JP, Dearth CL, Wolf MT, Ambrosio F, Boninger M, et al. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 2014;6:234ra58. https://doi.org/10.1126/scitranslmed.3008085.

    Google Scholar 

  172. Corona BT, Wu X, Ward CL, McDaniel JS, Rathbone CR, Walters TJ. The promotion of a functional fibrosis in skeletal muscle with volumetric muscle loss injury following the transplantation of muscle-ECM. Biomaterials. 2013;34:3324–35. https://doi.org/10.1016/j.biomaterials.2013.01.061.

    Google Scholar 

  173. Turner NJ, Badylak JS, Weber DJ, Badylak SF. Biologic scaffold remodeling in a dog model of complex musculoskeletal injury. J Surg Res. 2012;176:490–502. https://doi.org/10.1016/j.jss.2011.11.1029.

    Google Scholar 

  174. Wu X, Corona BT, Chen X, Walters TJ. A standardized rat model of volumetric muscle loss injury for the development of tissue engineering therapies. Biores Open Access. 2012;1:280–90. https://doi.org/10.1089/biores.2012.0271.

    Google Scholar 

  175. Garg K, Ward CL, Hurtgen BJ, Wilken JM, Stinner DJ, Wenke JC, et al. Volumetric muscle loss: persistent functional deficits beyond frank loss of tissue. J Orthop Res. 2015;33:40–6. https://doi.org/10.1002/jor.22730.

    Google Scholar 

  176. Corona BT, Machingal MA, Criswell T, Vadhavkar M, Dannahower AC, Bergman C, et al. Further development of a tissue engineered muscle repair construct in vitro for enhanced functional recovery following implantation in vivo in a murine model of volumetric muscle loss injury. Tissue Eng. Part A. 2012;18:1213–28. https://doi.org/10.1089/ten.tea.2011.0614.

    Google Scholar 

  177. Turner NJ, Yates AJ, Weber DJ, Qureshi IR, Stolz DB, Gilbert TW, et al. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng. Part A. 2010;16:3309–17. https://doi.org/10.1089/ten.tea.2010.0169.

    Google Scholar 

  178. Cofield RH, Parvizi J, Hoffmeyer PJ, Lanzer WL, Ilstrup DM, Rowland CM. Surgical repair of chronic rotator cuff tears. J. Bone Jt. Surgery, Am. 2001;83:71. https://doi.org/10.2106/00004623-200101000-00010.

    Google Scholar 

  179. Narayanan G, Nair LS, Laurencin CT. Regenerative engineering of the rotator cuff of the shoulder. ACS Biomater Sci Eng. 2018;4:751–86.

    Google Scholar 

  180. Ricchetti ET, Aurora A, Iannotti JP, Derwin KA. Scaffold devices for rotator cuff repair. J. Shoulder Elbow Surg. 2012;21:251–65. https://doi.org/10.1016/j.jse.2011.10.003.

    Google Scholar 

  181. Liu X, Manzano G, Kim HT, Feeley BT. A rat model of massive rotator cuff tears. J Orthop Res. 2011;29:588–95. https://doi.org/10.1002/jor.21266.

    Google Scholar 

  182. Cofield RH, Parvizi J, Hoffmeyer P, Lanzer WL, Ilstrup D, Rowland CM. Surgical repair of chronic rotator cuff tears: a prospective long-term study. 2001. doi:https://doi.org/10.2106/00004623-200101000-00010.

  183. Feeley BT, Rotator cuff muscle atrophy and fatty infiltration progress in understanding the underlying mechanisms. Am Acad Orthopadic Surg 2014.

  184. Gladstone JN, Bishop JY, Lo IKY, Flatow EL. Infiltration and atrophy of the rotator cuff do not improve after rotator cuff repair and. Am J Sports Med 2007;719–728. doi:https://doi.org/10.1177/0363546506297539.

  185. Dines JS, Bedi A, ElAttrache NS, Dines DM. Single-row versus double-row rotator cuff repair: techniques and outcomes. J Am Acad Orthop Surg. 2010;18:83–93.

    Google Scholar 

  186. Rodeo SA, Potter HG, Kawamura S, Turner AS, Kim HJ, Atkinson BL. Biologic augmentation of rotator cuff tendon-healing with use of a mixture of osteoinductive growth factors. J Bone Joint Surg Am. 2007;89:2485–97. https://doi.org/10.2106/JBJS.C.01627.

    Google Scholar 

  187. Prabhath A, Vernekar VN, Sanchez E, Laurencin CT. Growth factor delivery strategies for rotator cuff repair and regeneration. Int J Pharm. 2018;544:358–71.

    Google Scholar 

  188. Perry SM, Gupta RR, Van Kleunen J, Ramsey ML, Soslowsky LJ, Glaser DL. Use of small intestine submucosa in a rat model of acute and chronic rotator cuff tear. J Shoulder Elb Surg. 2007;16:179–83. https://doi.org/10.1016/j.jse.2007.03.009.

    Google Scholar 

  189. Thangarajah T, Henshaw F, Sanghani-Kerai A, Lambert SM, Blunn GW, Pendegrass CJ. The effectiveness of demineralized cortical bone matrix in a chronic rotator cuff tear model. J Shoulder Elb Surg. 2017;26:619–26. https://doi.org/10.1016/j.jse.2017.01.003.

    Google Scholar 

  190. Beason DP, Connizzo BK, Dourte LM, Mauck RL, Soslowsky LJ, Steinberg DR, et al. Fiber-aligned polymer scaffolds for rotator cuff repair in a rat model. J Shoulder Elb Surg. 2012;21:245–50. https://doi.org/10.1016/j.jse.2011.10.021.

    Google Scholar 

  191. Sean Peach M, Ramos DM, James R, Morozowich NL, Mazzocca AD, Doty SB, et al. Engineered stem cell niche matrices for rotator cuff tendon regenerative engineering. PLoS One. 2017. https://doi.org/10.1371/journal.pone.0174789.

  192. Yin Z, Heng BC, Feng G, Le H, Tang C, Huang J. Alignment of collagen fiber in knitted silk scaffold for functional massive rotator cuff repair. Acta Biomater. 2017;51:317–29. https://doi.org/10.1016/j.actbio.2017.01.041.

    Google Scholar 

  193. Hast MW, Zuskov A, Soslowsky LJ. The role of animal models in tendon research. Bone Joint Res. 2014;3:193–202. https://doi.org/10.1302/2046-3758.36.2000281.

    Google Scholar 

  194. Barton ER, Gimbel JA, Williams GR, Soslowsky LJ. Rat supraspinatus muscle atrophy after tendon detachment. J. Orthop. Res. 2005;23:259–65. https://doi.org/10.1016/j.orthres.2004.08.018.

    Google Scholar 

  195. Davis ME, Stafford PL, Jergenson MJ, Bedi A, Mendias CL. Muscle fibers are injured at the time of acute and chronic rotator cuff repair. Clin Orthop Relat Res. 2015;473:226–32. https://doi.org/10.1007/s11999-014-3860-y.

    Google Scholar 

  196. Rowshan K, Hadley S, Pham K, Caiozzo V, Lee TQ, Gupta R. Development of fatty atrophy after neurologic and rotator cuff injuries in an animal model of rotator cuff pathology. J Bone Joint Surg Am. 2010;92:2270–8. https://doi.org/10.2106/JBJS.I.00812.

    Google Scholar 

  197. Easley JT, Feeley B, Luan T, Liu X, Ravishankar B, Puttlitz C, et al. Muscle atrophy and fatty infiltration after an acute rotator cuff repair in a sheep model. Muscles. Ligaments Tendons J. 2015;5:106–12. https://doi.org/10.11138/mltj/2015.5.2.106.

    Google Scholar 

  198. Tang X, Khan Y, Laurencin CT. Biomimetic electroconductive scaffolds for muscle regenerative engineering. Adv Mater Lett. 2017;8:587–91. https://doi.org/10.5185/amlett.2017.7106.

    Google Scholar 

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Funding

The authors would like to acknowledge the NSF EFRI 1332329 and NIH DP1AR068147 and NIH RO1 AR063698 for funding this work (C.T.L.). Dr. Laurencin is a recipient of the National Medal of Technology and Innovation.

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Authors and Affiliations

  1. Connecticut Convergence Institute for Translation in Regenerative Engineering, UConn Health, Farmington, CT, 06030, USA

    Xiaoyan Tang, Leila Daneshmandi, Guleid Awale, Lakshmi S. Nair & Cato T. Laurencin

  2. Department of Orthopaedic Surgery, UConn Health, Farmington, CT, 06030, USA

    Xiaoyan Tang, Leila Daneshmandi, Guleid Awale, Lakshmi S. Nair & Cato T. Laurencin

  3. Raymond and Beverly Sackler Center for Biomedical, Biological, Physical and Engineering Sciences, UConn Health, Farmington, CT, 06030, USA

    Xiaoyan Tang, Leila Daneshmandi, Guleid Awale, Lakshmi S. Nair & Cato T. Laurencin

  4. Department of Materials Science and Engineering, University of Connecticut, Storrs, CT, 06269, USA

    Xiaoyan Tang, Lakshmi S. Nair & Cato T. Laurencin

  5. Department of Biomedical Engineering, University of Connecticut, Storrs, CT, 06269, USA

    Leila Daneshmandi, Lakshmi S. Nair & Cato T. Laurencin

  6. Department of Chemical and Biomolecular Engineering, University of Connecticut, Storrs, CT, 06269, USA

    Guleid Awale & Cato T. Laurencin

Authors
  1. Xiaoyan Tang
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  2. Leila Daneshmandi
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  3. Guleid Awale
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  4. Lakshmi S. Nair
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  5. Cato T. Laurencin
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Correspondence to Cato T. Laurencin.

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Tang, X., Daneshmandi, L., Awale, G. et al. Skeletal Muscle Regenerative Engineering. Regen. Eng. Transl. Med. 5, 233–251 (2019). https://doi.org/10.1007/s40883-019-00102-9

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